Relative Importance of Phosphodiesterase vs. Phosphomonoesterase (Alkaline Phosphatase) Activities for Dissolved Organic Phosphorus Hydrolysis in Epi- and Mesopelagic Waters

Abstract

Marine microbes use extracellular phosphatases to hydrolyze phosphate from organic matter. Dissolved organic phosphorus (DOP) is typically present in higher concentrations than phosphate in oceanic surface waters. Yet, the fate and role of different DOP components, such as phosphomonoester and phosphodiester, are poorly understood. Most of the investigations on extracellular enzymatic hydrolysis of marine DOP have focused on phosphomonoesterase (MEA) activity (i.e., alkaline phosphatase), whereas phosphodiesterase (DEA) measurements are scarce. This limits our understanding of the ecological and biogeochemical role of DOP sources other than P-monoesters in the sea. We determined extracellular MEA and DEA activities including their cell-free fractions on a bimonthly basis over 14 months in surface and mesopelagic subantarctic waters, thus covering a wide range of phosphate availability levels (from <0.5 to 2.3 µM). We found that DEA and MEA exhibit similar hydrolysis rates in surface as well as in mesopelagic waters. The MEA:DEA ratio varied between 0.38 and 5.42 during the study period, indicating potential differences in function and/or expression among the two enzyme groups, potentially reflecting differences in the availability and/or utilization of P-monoester and P-diester pools. Interestingly, the MEA:DEA was negatively correlated to phosphate (r −0.82, p 0.02, R 2 0.67) and positively with the inorganic N:P ratio (r 0.84, p 0.02, R 2 0.67), suggesting that the relative importance of DEA vs. MEA is linked to inorganic P availability and the N:P ratio. DEA was also related to the N:P ratio, both at the surface and at depth, suggesting DEA alone is sensitive to changes in the N:P ratio. The majority (>70%) of extracellular MEA and DEA was found in the cell-free fraction, increasing with depth for MEA. Our results indicated that DOP hydrolysis mediated by DEA in the surface as well as in dark ocean is as important as the frequently measured MEA.

Phosphomonoesterase and phosphodiesterase activities in the Eastern Mediterranean Sea during stratified versus mixed conditions

“…From studies were both phosphatase rates were available (Sato et al, 2013;Thomson et al, 2019) as well in our study, both PDE and PME maximum rates were one the same order of magnitude and their variability was much better explained by DIP concentrations than by DOP or LDOP concentrations. In Thomson et al (2020) study, the ratio of rates PME:PDE in surface was lower or higher than 1 (range 0.5 to 5.3) and varied seasonally. Their surface values were correlated negatively with DIP and positively with the NOx:DIP ratio.…”

“…After enrichment of various chemical forms of organic phosphate added experimentally, the high changes in taxonomic diversity and activity of heterotrophic bacteria and phytoplankton (Muscarella et al, 2014;Sisma-Ventura and Rahav, 2019;Filella et al, 2022) as well as expression of different phosphatase genes (Zheng et al, 2019), suggest a strong role of the DOP availability in shaping microbial diversity in aquatic environments. Nevertheless, if PDE has been already measured in environmental conditions in eutrophic aquatic systems (Jorgensen et al, 2015) or coastal area (Huang et al, 2022), few studies describe PDE activity in oceanic waters, and only in the Pacific Ocean (Sato et al, 2013;Yamaguchi et al, 2019;Thomson et al, 2020;Srivastava et al, 2021).…”

Seasonal Prokaryotic Community Linkages Between Surface and Deep Ocean Water

“…The Munida transect spans the waters associated with the subtropical front (STF) in the South Pacific Ocean off the South Island of New Zealand. The Munida time series transect was established in 1998 to investigate long term changes in carbonate chemistry, but since then several other works have taken place and sampling for MOTS began in 2014 (Currie and Hunter, 1999;Currie et al, 2011;Brix et al, 2013;Jones et al, 2013;Baltar et al, 2015Baltar et al, , 2016Morales et al, 2018;Thomson et al, 2019Thomson et al, , 2020Allen et al, 2020). The transect extends 65 km offshore and encompasses coastal neritic waters, modified subtropical waters of the Southland Current, the STF and subantarctic waters (SAW) (Jillett, 1969).…”

Phosphorus cycling in the upper waters of the Mediterranean Sea (PEACETIME cruise): relative contribution of external and internal sources

“…Other organic P compounds such as phosphate diesters or phosphonates are known to provide alternative sources of P (Dyhrman et al, 2006;Whitney and Lomas, 2019;Thomson et al, 2020).…”